Auxin receptors as integrators of developmental and hormonal signals during reproductive development in pea

Abstract

Auxins regulate many aspects of plant growth and development. In pea, three of the five TIR1/AFB members (PsTIR1a, PsTIR1b, PsAFB2) have been implicated in auxin-related responses during fruit/seed development; however, the roles of PsAFB4 and PsAFB6 in these processes are unknown. Using yeast two-hybrid assays, we found that all five pea TIR1/AFB receptor proteins interacted with pea AUX/IAAs PsIAA6 and/or PsIAA7 in an auxin-dependent manner, a requirement for functional auxin receptors. All five auxin receptors are expressed in young ovaries (pericarps) and rapidly developing seeds with overlapping and unique developmental and hormone-regulated gene expression patterns. Pericarp PsAFB6 expression was suppressed by seeds and increased in response to deseeding, and exogenous hormone treatments suggest that seed-derived auxin and deseeding-induced ethylene are involved in these responses, respectively. Ethylene-induced elevation of pericarp PsAFB6 expression was associated with 4-Cl-IAA-specific reduction in ethylene responsiveness. In developing seeds, expression of PsTAR2 and PsYUC10 auxin biosynthesis genes was associated with high auxin levels in seed coat and cotyledon tissues, and PsAFB2 dominated the seed tissue transcript pool. Overall, auxin receptors had overlapping and unique developmental and hormone-regulated gene expression patterns during fruit/seed development suggesting mediation of diverse responses to auxin, with PsAFB6 linking auxin and ethylene signaling.

Auxins in the right space and time regulate pea fruit development

“…In pea, the higher bioactivity of 4-Cl-IAA compared with IAA was recognized and studied already early on ( Reinecke et al , 1995 ; Magnus et al , 1997 ); however, without having the possibility to knock out only one pathway by identifying the halogenation step, this still remained a point of discussion. Reinecke et al (1999) first hypothesized that the binding to the receptor complex should favour the 4-Cl derivative using structure–activity studies, and this hypothesis is further supported by the receptor characterization in Ozga et al (2022) . Deseeded pericarps have been used to partially answer the question about the effect of the two auxins since they can be supplemented with either auxin and then the growth response analysed.…”

“…The perception of auxin is essential, especially in pea plants where two types of auxin are present, and the chlorinated form seems to be the more active one. The elegant and detailed work by Ozga et al (2022 ) has shown how indole-3-acetic acid (IAA), 4-chloro-indole-3-acetic acid (4-Cl-IAA), gibberellin (GA), and ethylene contribute to pea seed development by dissecting the different tissues for the analysis of the response in addition to the interaction of pea auxin receptors with the Aux/IAA repressors, and identified a complex tissue-specific hormonal network.…”

“…The transcriptional activation via ARF proteins can then take place (right). Experimental evidence was reported for the physical binding of 4-Cl-IAA and IAA to all pea auxin receptors by Ozga et al (2022) . The pea plant cartoon is from BioRender (free version: https://biorender.com/ ; accessed 5.5.2022).…”

“…Transcription can start only then since the ARF-type activators can bind to the promoter of auxin-responsive genes ( Ulmasov et al , 1997 ). The analysis of the sequences for auxin perception in pea has revealed the occurrence of six genes that encode putative auxin receptors and potentially bind with higher affinity to 4-Cl-IAA than to IAA ( Ozga et al , 2022 ). The work by Ozga et al (2022) , being the latest research in a series of publications on the same topic ( Johnstone et al , 2005 ; Jayasinghege et al, 2017 , 2019 ), has tremendously advanced the field by combining different tissues and their dissection into smaller functional parts with different methods such as treatment with hormones, molecular interaction assays, and transcript and hormone analyses.…”

“…The analysis of the sequences for auxin perception in pea has revealed the occurrence of six genes that encode putative auxin receptors and potentially bind with higher affinity to 4-Cl-IAA than to IAA ( Ozga et al , 2022 ). The work by Ozga et al (2022) , being the latest research in a series of publications on the same topic ( Johnstone et al , 2005 ; Jayasinghege et al, 2017 , 2019 ), has tremendously advanced the field by combining different tissues and their dissection into smaller functional parts with different methods such as treatment with hormones, molecular interaction assays, and transcript and hormone analyses. Overall, the results of this challenging work show a developmental regulation of auxin receptor genes as well as genes for auxin biosynthesis and hormone levels in seedling and fruit tissues.…”